Biomphalaria and Bulinus Spp

Acta Tropica 132 (2014) 64–74

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Acta Tropica

jo urnal homepage: www.elsevier.com/locate/actatropica

Regulation of laboratory populations of snails (Biomphalaria and

Bulinus spp.) by river prawns, Macrobrachium spp. (Decapoda,

Palaemonidae): Implications for control of schistosomiasis

a,∗,1 b a

Susanne H. Sokolow , Kevin D. Lafferty , Armand M. Kuris

Ecology Evolution and Marine Biology Department, University of California Santa Barbara, Santa Barbara, CA, 93106, USA

Western Ecological Research Center, US Geological Survey, c/o Marine Science Institute, University of California, Santa Barbara, CA, 93106, USA

a r a

t i c l e i n f o b s t r a c t

Article history: Human schistosomiasis is a common parasitic disease endemic in many tropical and subtropical

Received 29 October 2013

countries. One barrier to achieving long-term control of this disease has been re-infection of treated

Received in revised form

patients when they swim, bathe, or wade in surface fresh water infested with snails that harbor and

13 December 2013

release larval parasites. Because some snail species are obligate intermediate hosts of schistosome para-

Accepted 19 December 2013

sites, removing snails may reduce parasitic larvae in the water, reducing re-infection risk. Here, we

Available online 31 December 2013

evaluate the potential for snail control by predatory freshwater prawns, Macrobrachium rosenbergii and

M. vollenhovenii, native to Asia and Africa, respectively. Both prawn species are high value, protein-rich

Keywords:

Predation human food commodities, suggesting their cultivation may be beneﬁcial in resource-poor settings where

few other disease control options exist. In a series of predation trials in laboratory aquaria, we found both

Biological control

Functional response species to be voracious predators of schistosome-susceptible snails, hatchlings, and eggs, even in the pres-

Predator ence of alternative food, with sustained average consumption rates of 12% of their body weight per day.

Schistosoma mansoni Prawns showed a weak preference for Bulinus truncatus over Biomphalaria glabrata snails. Consumption

Schistosoma haematobium

rates were highly predictable based on the ratio of prawn: snail body mass, suggesting satiation-limited

predation. Even the smallest prawns tested (0.5–2 g) caused snail recruitment failure, despite high snail

fecundity. With the World Health Organization turning attention toward schistosomiasis elimination,

native prawn cultivation may be a viable snail control strategy that offers a win–win for public health

and economic development.

1. Introduction surface fresh water. A few weeks after infection, snails release larval

schistosomes into the water where they can infect people, comple-

Human schistosomiasis is a common parasitic disease of ting the lifecycle. Breaking this lifecycle through snail control was

humans that is relatively easy to treat, but hard to control. Today, an approach used extensively for schistosomiasis control prior to

public health campaigns in endemic regions in the tropics and the advent of the drug praziquantel. Snail control aims to reduce

subtropics focus on mass drug administration using the oral drug, the number of parasitic larvae in the water, effectively reduc-

praziquantel. While praziquantel has a high cure rate, re-exposure ing reinfection prevalence and intensity. Traditional approaches

to infected snails in the environment leads to rapid reinfection of to snail control using molluscicide application and habitat mod-

treated patients in endemic areas (Fenwick et al., 2006; Fenwick iﬁcation can be expensive to implement and hard to maintain

and Webster, 2006; King et al., 2006; Tchuem Tchuente et al., over the long-term. In some areas, researchers have documented

2013; Webster et al., 2013). In addition to drug treatment, a a negative relationship between natural aquatic snail predators

complementary approach is to control the populations of snails and the density of schistosome-susceptible snails, such as occurs

that serve as intermediate hosts. Snails are infected when para- in regions of Lake Malawi, where overﬁshing pressure may have

site eggs, released in human urine or feces, are washed into the caused snail populations to increase after predators were removed

(Evers et al., 2006; Madsen and Stauffer, 2011). This suggests that

in some ecological situations, control of snails through predator

introductions could offer an effective snail control strategy that

∗

Corresponding author at: Stanford University, Hopkins Marine Station, 20

is affordable and sustainable and that may complement ongo-

Oceanview Blvd, Paciﬁc Grove, CA 93950, USA. Tel.: +1 831 5153205..

ing drug distribution campaigns. Here, we evaluate the potential

E-mail address: [email protected] (S.H. Sokolow).

1 for snail control by predatory freshwater prawns in the genus

Present afﬁliation: Stanford University, Hopkins Marine Station, Paciﬁc Grove,

CA 93950, USA. Macrobrachium.

S.H. Sokolow et al. / Acta Tropica 132 (2014) 64–74 65

Macrobrachium vollenhovenii, is a freshwater prawn native to characterize the functional response of prawns when offered vary-

rivers and streams throughout West Africa. We hypothesized that ing sizes and densities of snails, as would be found in natural

M. vollenhovenii would be an effective snail predator because this populations. Finally, we aimed to synthesize this information to

species shares similar habitats with medically important snails, guide the development of a new strategy for sustainable schistoso-

grows to a large size, and because the congener Macrobrachium miasis control and elimination through restoration or stocking of

rosenbergii (an Asian species) consumes snails as a preferred food river prawns in schistosomiasis-endemic areas, especially through-

(Lee et al., 1982; Roberts and Kuris, 1990). In Senegal, the con- out Africa where the highest schistosomiasis transmission rates are

struction of the Diama Dam to block tidal inﬂuence in the Lower found today.

Senegal River created a large freshwater irrigation system that

offered abundant habitat to medically important snails, hosts of

2. Methods

both Schistosoma mansoni and Schistosoma haematobium. This was

associated with a severe and persistent outbreak of schistosomia-

2.1. Animals

sis involving both species, with increased snail abundance resulting

from expanded low-ﬂow, freshwater snail habitat after dam com-

Uninfected, laboratory-reared Biomphalaria glabrata, strain

pletion as well as probable immigration of infected agricultural

NMRI, and Bulinus truncatus, subspp. truncatus, were supplied by

workers to the region (Southgate, 1997; Sow et al., 2002). The

the Schistosomiasis Resources Center (BEI Resources, Manassas,

Diama Dam also presumably blocked the migration of native M.

VA). Laboratory-reared M. rosenbergii juvenile prawns were sup-

vollenhovenii prawns to their estuarine breeding grounds. Although

plied by the Aquaculture Department at Kentucky State University

other impacts of the dam were not investigated, local ﬁshermen

and delivered by airfreight to the University of California Santa

reported that prawns were once common, but declined sharply

Barbara. Captive populations of M. vollenhovenii prawns were not

after dam construction. Since prawns have been shown in labora-

available, so wild-caught prawns were collected from the Lobe

tory studies to be voracious and effective predators of Biomphalaria

River, Cameroon (Gulf Aquatics-Cameroon, Duoung, Cameroon)

glabrata (Lee et al., 1982; Roberts and Kuris, 1990), we speculate

and delivered by air freight in December 2011 to Kentucky

that a loss of prawns above Diama Dam may have contributed to

State University’s Aquaculture Department. At Kentucky State,

the increase in snail intermediate hosts in the Lower Senagal River

the prawns were captively bred and the ﬁrst generation juve-

Basin, and therefore, an increase in schistosomiasis transmission. If

nile prawns were delivered by airfreight to UC Santa Barbara in

so, restoration of M. vollenhovenii to the Senegal River might con-

June 2012. Prawns and snails were housed in closed, recirculat-

tribute to schistosomiasis control in that region or other similar

ing freshwater tanks at UC Santa Barbara’s Marine Biotechnology

regions of the world where schistosomiasis has increased after dam

Laboratory. The tank system had both mechanical and biological

construction (Steinmann et al., 2006).

ﬁltration, continuous aeration, and 20% weekly water exchanges

Roberts and Kuris (1990) published a series of laboratory tri-

using conditioned tap water. Between experiments, prawns and

als that built on earlier work (Lee et al., 1982) demonstrating that

snails were housed in holding tanks: a 400 L common holding tank

M. rosenbergii – the most commonly aquacultured species of fresh-

for prawns, and four 25 L holding tanks for snails. Both during

water prawn worldwide – can consume B. glabrata snails. Roberts

and between experiments, prawns were fed a commercial shrimp

and Kuris concluded that prawn cultivation may offer a valuable

crumble diet with 40% protein content (Rangen Corporation, Buhl,

complementary strategy for schistosomiasis control activities. Yet,

ID) at a rate of 3–5% body weight per day, 5 days per week, and

to date, biological control using crustacean snail-predators has not

snails were fed organic romaine lettuce rinsed in DI water, ad libi-

been widely applied within schistosomiasis control programs. One

tum. In some trials, snails also fed on the shrimp diet (see below

of the major barriers to adoption is the lack of safe and effec-

for details). Experiments were conducted in individual, clear poly-

tive native species for biological control. Introducing exotic species

ethylene tanks with plastic lids, ﬁlled to 6 L with conditioned tap

into habitats where they have never been previously naturalized

water, and connected by PVC and vinyl plumbing in a closed recir-

can cause unwanted effects (Barbaresi and Gherardi, 2000; Fishar,

culating freshwater tank system. Tanks each had a single simulated

2006; Lodge et al., 2012). Nevertheless, there are a few exam-

prawn habitat refuge (a section of PVC pipe). Prawns were fasted,

ples where the introduction of exotic crustacean predators was

and all snails removed, for at least 24 h between trials to prevent

successful in controlling schistosomiasis. For example, in Kenya,

cross-trial carryover effects.

the introduction of a previously naturalized exotic crustacean, the

Louisiana crayﬁsh Procambarus clarkii, to village impoundments

signiﬁcantly reduced the prevalence and intensity of S. haemato- 2.2. Measuring consumption in terms of snail number versus

bium in schoolchildren for at least two years (Mkoji et al., 1999). snail biomass

Some additional evidence is emerging to suggest that invasions

of this species throughout the Nile Delta may inﬂuence the rates In all experiments, consumption was measured and reported

of schistosomiasis transmission there (Khalil and Sleem, 2011). in terms of snail number, snail biomass, or both. For the most

We argue that native predator augmentation would be similarly part, we focused on the number of snails eaten by prawns because

beneﬁcial for schistosomiasis control programs while minimizing of its relevance to biological control of parasite transmission:

unwanted non-target effects associated with exotic introductions. The number (not biomass) of infected snails determines trans-

Here, we examine the long-term (days) consumption rates and mission risk to humans throughout a transmission season. This

characterize the functional response of two prawn species: M. vol- is due to the several-month average lifespan of schistosome-

lenhovenii and M. rosenbergii feeding on two species of snails B. susceptible snails, along with the long pre-patency and patency

glabrata (a host of S. mansoni) and Bulinus truncatus (a host of periods and the fact that small snails can be more susceptible

S. haematobium). Our goals were: (1) to assess the capacity for to infection (Barbosa, 1963; Loreau and Baluku, 1987; Niemann

prawns – especially the African native M. vollenhovenii for which and Lewis, 1990; Pﬂuger, 1980; Pﬂuger et al., 1984; Woolhouse

there were no previous data – to control laboratory populations of and Chandiwana, 1990a, 1990b). Thus, we measured consumption

Biomphalaria and Bulinus snails, hosts for human schistosomes in mainly in terms of the number of snails consumed/time or, where

Africa and the Americas; (2) to compare the predation rates and appropriate, the number consumed/gram-prawn-biomass/time. A

preferences of small juvenile prawns versus large adult prawns second beneﬁt of focusing on the number of snails consumed was

and between Malaysian and African prawn species; and (3) to to allow comparison with other studies, since we used the classic

66 S.H. Sokolow et al. / Acta Tropica 132 (2014) 64–74

Holling’s Type II functional response equation, which deﬁnes two masses were tested, based on availability: M. rosenbergii ranged

aggregate parameters that govern the overall shape and asymptotic from 0.3 g to 130 g and M. vollenhovenii ranged from 0.3 g to

maximum of the functional response curve, typically expressed in 20 g.

terms of prey number over a range of prey densities (not biomass). For some analyses, prawns were split into size classes, with a

In a few cases, it was logical to report consumption in terms of cut-off above 30 g body mass signifying a full “market” size (tar-

both snail number and biomass (e.g., in the preference trials) or to get size at harvest) (New and Valenti, 2000). There were ﬁve size

focus on biomass alone. For example, for comparisons of consump- classes for prawns: XS (0.3–1 g), S (1–3 g), M (3–10 g), L (10–30 g),

tion patterns among prawn species, we focused solely on biomass Market (>30 g). A total of 3 to 6 (median 5) replicate prawns of

as a measure of consumption because this is the most important each species/size-class were tested in each snail-size/-species/-

factor from the predator’s perspective. Digestion is the most com- density combination, and each replicate 12-h trial was repeated

mon limiting factor regulating consumption rates among predators, 4–6 consecutive times, for a total of 48–72 h of observation with

including crustaceans (Jeschke et al., 2002; Konan et al., 2010). We replacement of consumed snails every 12 h. Trials were conducted

therefore hypothesized that over relatively long time spans (days), within three banks of nine 10 L tanks, each bank with a common

prawns would satiate based on the total biomass consumed, com- sump, pump, and ﬁltration. In order to complete all replicates,

pared with the capacity of their gastrointestinal tracts, and that batches of trials were conducted longitudinally through time, with

they would satiate more quickly when feeding on large versus small the order of the snail-size/-species/-density combinations random-

snails, making the biomass of snails a more tractable and consistent ized through time and among tanks. One to three control tanks

predictor of satiation than the number of snails consumed, in this containing snails but no prawns were monitored during each trial.

speciﬁc case. In all statistical tests, we used an alpha level of 0.05. The number of snails offered, the number consumed, and the num-

ber of empty shells was recorded every 12 h.

2.3. Experiment 1—Preference trials We compared predation rates of the two prawn species within

their overlapping size range (2–26 g). We assumed that predation

Preference for Biomphalaria or Bulinus spp. was assessed for ﬁve rates would follow from metabolic requirements of growth, which

replicate M. rosenbergii prawns (size range: 9.6–77 g) offered equal for Macrobrachium spp. follow a Von Bertalanffy growth curve

numbers of each snail species (ﬁrst in a ratio of 20:20 snails, then (Etim and Sankare, 1998; Gabche and Hockey, 1995) and thus there

repeated with a ratio of 40:40 snails). Similar trials were repeated to would be a predictable relationship between prawn size and con-

assess size-preferences using Biomphalaria single-species assem- sumption rate. We thus calculated the biomass of snails consumed

blages, examining preferences of large and small M. rosenbergii (per gram prawn) in each trial and used a cube-root transforma-

prawns (size range: 0.5–77 g) consuming snails in three size classes: tion to linearize the relationship, based on the Von Bertalanffy

small (4 mm ± 2 mm shell diameter), medium (8 mm ± 2 mm), and growth equations and published length–weight relationships for

large (12 mm ± 2 mm) at equal densities (1:1:1). each species (King et al., 2005; Sandbach, 1976). This allowed a sim-

At the start of each preference trial, all snails were weighed ple comparison of consumption by size patterns between the two

and measured. At each daily observation point, all remaining snails prawn species via a comparison of the slopes of the regression lines.

were again weighed, measured, and returned to the tanks until To assess the differences among species, we compared the slope of

all of the snails had been consumed. Data were analyzed using a the regression line for prawn length (size) versus linearized con-

selectivity index calculated for each replicate prawn at each obser- sumption rate using ANCOVA, with snail length and snail density

vation point excluding those observation points at which no snails as additional covariates. After ﬁnding no differences between con-

remained (Eq. (1)). The selectivity index (SI) was calculated as fol- sumption rates for the two prawn species (see results, below and

lows: Fig. 1; ANCOVA on linearized data: p = 0.53), the data were pooled

across species and the remainder of the analyses of consumption

ni/ntot

SI (1) rates and functional response were based on the full range of trials

oi/otot

for M. rosenbergii (0.5 g to 130 g) and M. vollenhovenii (0.3 g to 20 g)

where ni/ntot was the fraction of snails consumed that were species together.

(or size class) i and oi/otot was the fraction offered that were species The effects of prawn size and snail size on the (log-transformed)

(or size class) i during that observation period. Under conditions of consumption rates were tested using a linear mixed model imple-

random selection (no preference), the expected value of this index mented in JMP version 10 (SAS Institute Inc., Cary NC, USA) with

is 1. Selectivity indices were calculated by number of snails and by individual prawns included as a random effect (due to the fact

biomass of snails. Bootstrapped conﬁdence intervals for this index that individual prawns were measured repeatedly). Trials in which

were calculated in R.2.15.2 (CRAN http://cran.us.r-project.org/) prawns were molting were excluded because prawns typically fast

using 999 bootstrap replicates in the “boot” function of the R base during the molt (Roberts and Kuris, 1990).

package. In order to quantify the functional responses to changing snail

density, we estimated a classic Holling’s Type II functional response

2.4. Experiment 2—Predation rates and functional response curve (Eq. (2)) for each prawn-species/-size and snail-species/-size

combination:

In order to quantify the daily consumption rates and

characterize the functional response, prawns were housed aN

N = o

individually and offered varying densities of snails, with replace- e (2)

1 + aThNo

ment every 12 h, for 72 h. During all trials, prawns were fed

their normal ration of pelleted shrimp diet calculated by dry

weight and fed daily at 3–5% of prawn wet weight per day. where Ne is the number of snails eaten, No is the number (den-

Snails were size-sorted so that prawns were offered small sity) offered per tank, a is the per capita attack rate, and Th is

(4 mm ± 2 mm shell length), medium (8 mm ± 2 mm), or large the “handling time” parameter. Parameters were estimated from

(12 mm ± 2 mm) Biomphalaria glabrata, or one-size-class (5–10 mm the data by non-linear least squares ﬁtting of Eq. (2) in JMP ver-

shell length) Bulinus truncatus. M. rosenbergii were offered sion 10. Conﬁdence bounds for each parameter were determined

either 6, 12, 24, or 48 snails/tank, and M. vollenhovenii 12 using bootstrapping, via 999 bootstrapped replicates in the “boot”

and 24 snails/tank for comparison. Prawns of a range of body function of the R base package.

S.H. Sokolow et al. / Acta Tropica 132 (2014) 64–74 67

days. Ten large (>10 mm shell length) adult snails of either B.

glabrata or B. truncatus were added to each tank as founder popula-

10 tions. Snails were weighed and measured at the start and fed lettuce

ad libitum throughout the study. Snails were left to acclimate and

lay eggs for 7 days at the start of the experiment. Then, prawns

were introduced into half the tanks (at a density of 3 prawns per

tank, each prawn <2 g) and all tanks were monitored every 5–7

days until the termination of the experiment. At each observa-

0.7

0.5 tion point, all remaining adult snails were counted, and any dead

0.3 snails were removed and replaced to simulate an open population

0.2 of adult snails at equilibrium densities, where any loss of an adult

snail would likely lead to an opportunity for replacement by an

0.1

0.07 immigrant snail into that habitat. The number of egg masses and

0.05

the number of recruit snails in the hatchling, juvenile, and adult

0.03

size classes – which were deﬁned as <4 mm, 4–8 mm, and >8 mm

0.02

shell length, respectively, for Biomphalaria and <3 mm, 3–6 mm,

Biomass (g) snails consumed/prawn/day

0.01 and >6 mm shell length, respectively, for Bulinus – were counted at

0.007

each observation point. The population trajectories for snail popu-

0.4 0.7 1 2 3 4 5 7 10 20 40 60 100 200 lations in the presence and absence of prawns were plotted over

Prawn weight (g) time and the means were compared at the midpoint and endpoint

using repeated measures ANOVA.

Fig. 1. Comparing consumption rates for two prawn species: M. rosenbergii (ﬁlled

circles) and M. vollenhovenii (open triangles). The dashed line represents the “line

of equivalence,’ or a constant 12% consumption rate over all body sizes which was 2.7. Experiment 3c—Comparing the effect of prawns with the

the average overall consumption rate (it is not a regression line). Points above the

effects of food supplementation & manual removal of juvenile

line represent trials in which prawns ate more than the average of 12% of their snails

body weight daily and those falling below the line ate less than 12%. Each point

and vertical bar represents the average and standard error of multiple consecutive

consumption trials with a single prawn. Trials where prawns were offered single- Because it was noted that snail fecundity remained very high in

species populations of either B. glabrata (three size classes) or B. truncatus (one size the presence of prawns, a second experiment was conducted to iso-

class) were combined to generate this ﬁgure.

late a number of possible competing inﬂuences on the number of

egg masses that accumulated in tanks over time: effects of shrimp

feed supplementation (which the snails consumed), loss of recruit

2.5. Experiment 3a—Regulation of laboratory populations of

snails via predation – which was hypothesized to increase egg num-

Biomphalaria glabrata snails by very large prawns

bers via reduced egg cannibalism by recruit snails (i.e. a cannibalism

effect) or reduced competition for food resources between adult

Here, we built on the work of Roberts and Kuris (1990), which

and juvenile snails (i.e. a crowding effect) – or other effects associ-

showed that dense laboratory populations of B. glabrata could be

ated with prawn presence such as chemical/visual cues that could

consumed by predation in 20 days by individually-housed medium

have inﬂuenced hatching rates. Single-species laboratory popula-

sized (3–10 g) prawns. We repeated their experiments using very

tions of Biomphalaria snails were again established in nine tanks,

large market-sized prawns to compare the rate at which the largest

as before, using 10 large (>10 mm shell length) snails as founders

prawns (>30 g) could eliminate densely-populated mixed-sized

in each tank, and four treatments were applied as follows. Eight

populations of snails in the laboratory. Three large prawns (45 g,

tanks were offered equal weights of shrimp feed plus lettuce ad

56 g, and 72 g) were individually housed with 80 B. glabrata snails

libitum added daily and one tank served as a negative control (with

each, 20 snails from each of four size classes (4 mm, 8 mm, 12 mm,

only lettuce fed ad libitum, as in the previous experiment). In four

and 16 mm, all ±2 mm) after Roberts and Kuris (1990). Two control

of the eight tanks given shrimp feed supplementation, a single

tanks in the same ﬂow-through system were set up with a founder

prawn (0.5 g to 1.5 g) was added. In two of the remaining four tanks

population of 10 adult snails per tank (>10 mm) but no prawns. All

without prawns, all recruit snails that hatched from the eggs were

snails were weighed and measured at the start and monitored until

manually crushed (to simulate predation) and removed weekly. All

no snails remained in the prawn tanks.

tanks were again monitored every 5–7 days for 63 days, recording

the number of egg masses, the number of original founding adults

2.6. Experiment 3b—Regulation of laboratory populations of

remaining alive (replaced if dead or missing), and the number and

Biomphalaria and Bulinus snails by small prawns

sizes of snail recruits. The population trajectories were plotted over

time and the means compared at the midpoint and endpoint via

Although Macrobrachium spp. prawns can consume high num-

repeated measures ANOVA tests.

bers of snails, our results and previous studies (Roberts and Kuris,

1990) suggested that there exists a size refuge for large adult snails

faced with very small prawn (<2 g) predators. Yet, we suspected 3. Results

that small prawns would consume eggs and hatchling snails, lead-

ing to snail population regulation despite the size refuge. Due to 3.1. Comparing prawn species

the difﬁculty in handling and weighing very small hatchling snails

less than 1 mm in diameter, rather than directly manipulating snail No differences in consumption patterns were detected among

densities, we opted to address this question by monitoring snail the two prawn species, M. vollenhovenii and M. rosenbergii, despite

population recruitment rates among laboratory snail populations these two species originating from different continents, Africa and

through time in the presence or absence of very small prawns. Asia, respectively (Fig. 1; ANCOVA on linearized data: p = 0.53). This

To test whether small M. vollenhovenii prawns could achieve suggests that our results may be generalizable among both of these

population regulation despite their inability to consume adult prawn species. Although no other species were tested here, there

snails, snail populations were established and monitored for 90 are other large-bodied species with similar morphology among the

68 S.H. Sokolow et al. / Acta Tropica 132 (2014) 64–74

80 small prawn 2-3g A 5.5 70 medium prawn 7-12g 5.0 60 market-sized prawn 45-72g 4.5 50 4.0 40 3.5 30 3.0 20 2.5 10 2.0 Number of snails remaining/tank 0 rate/g Consumption 1.5 0 10 20 30 40 50 60 70

(# of snails/gram-prawn/day) (# of snails/gram-prawn/day) 1.0 days

0.5

Fig. 2. Consumption and elimination of high-density mixed-sized populations of 0.0

B. glabrata snails (80 snails/tank) by small M. rosenbergii prawns (2–3 g; circles), 0.02 0.03 0.050.07 0.1 0.2 0.3 0.4

medium M. rosenbergii prawns (7–12 g, triangles) and very large M. rosenbergii

prawns (>30 g, squares). Data for small and medium prawns are from Roberts and Average snail weight (g)

Kuris (1990); data for very large prawns are from this study. B 20

more than 240 species in the genus Macrobrachium distributed

throughout the world (De Grave and Fransen, 2011), many of which 14

occur where schistosomiasis is endemic, and tests of snail predation 12

among many of these species may be warranted. 8 6 4

Consumption rate Consumption

3.2. Predation rates 2

(# of snails/prawn/day) 0

Prawns consumed, on average, 12% (CI = 10.7–14.1%) of their 4.5

4.0

body weight in snail biomass per day. Predation rates varied consid-

3.5

erably among individual prawns on individual days, ranging from

3.0

0% to more than 90% of their body weight in snail tissue killed daily

2.5

(snail tissue = snail wet weight excluding shell weight). Although

2.0

prawn predation behavior was not formally recorded in these

1.5

experiments, many instances of prawn predation on snails were

1.0

directly observed. Prawns were often observed attacking snails by

Consumption rate/g Consumption 0.5

ﬁrst apprehending the snails using their ﬁrst pair of pareiopods

(# of snails/gram-prawn/day) (# of snails/gram-prawn/day) 0.0

(walking legs) and then lifting the snails to their mouthparts and XS S M L Market

crushing the shells using their mandibles, consuming the tissue Prawn size

and discarding (though sometimes consuming) the leftover shell.

In most cases, small prawns would not attack snails that were more Fig. 3. The effect of (A) snail size and (B) prawn size on snail consumption rates by

prawns. XS = <1 g prawns; S = 1–3 g prawns; M = 3–10 g prawns; L = 10–30 g prawns;

than 1/3 their own body weight, although small prawns were occa-

Market = >30 g prawns. Data from both M. rosenbergii and M. vollenhovenii preying

sionally directly observed killing very large snails by picking at snail

on snails of either B. glabrata or B. truncatus were combined to generate this ﬁgure.

tissue through the shell aperture without crushing the shell.

Prawn size (p = 0.0003) and snail size (p < 0.0001) were sig-

niﬁcantly associated with consumption rates based on the linear 3.3. Preference

mixed effects model results. The interaction between prawn size

and snail size was not signiﬁcant (p = 0.26). Larger prawns gen- By comparing the observed and expected selectivity indices

erally consumed the most snails and depleted high density snail and their conﬁdence intervals, calculated for each snail species

populations faster than smaller prawns (Figs. 2 and 3). Large M. (or size category), we assessed whether any preferences could be

rosenbergii prawns presented with dense, mixed-sized snail popu- detected. Signiﬁcant preferences were demonstrated if the entire

lations (experiment 3a) consumed all sizes of snails presented conﬁdence interval was greater than one, while indices with con-

to them, and completely eliminated snails from the tanks within ﬁdence intervals entirely less than one demonstrated signiﬁcant

an average of 10.4 days (range 7–21 days, Fig. 2). This extends avoidance. Small, but not large, prawns preferred small snails and

previous ﬁndings by Roberts and Kuris for 7–12 g M. rosenbergii avoided large ones (Fig. 4). The average wet weight of the largest

prawns that could deplete the same number of snails within c.a. B. glabrata snails was an order of magnitude larger, 0.31 ± SE 0.01 g

20 days (Fig. 2). However, on a gram per gram basis, prawn size (range: 0.16–1.06 g), than the wet weight of the smallest size class,

class was signiﬁcantly, non-linearly related to consumption rates 0.022 ± SE 0.001 g (range: 0.01–0.05 g). However, it should be noted

with smaller sized prawns having higher killing efﬁciency per gram that even the smallest snail size class offered here (4 mm ± 2 mm

(Fig. 3, p = 0.0004 by Wilcoxon test). Because prawns are territorial shell length) was still of a sufﬁcient size to be susceptible to schis-

and can be stocked at much higher densities when they are smaller, tosome infection (Anderson et al., 1982). In contrast, the largest,

this suggests that prawns of small to intermediate mass (1–30 g) market-sized prawns showed no clear size preferences in the snails

may be optimal for snail control. Prawns of all sizes could consume they would attack and kill (Fig. 4).

more small snails than large ones when presented with single-sized When M. rosenbergii prawns were offered mixed-species assem-

populations of snails, likely due to satiation effects (Fig. 3). blages of snails, there was a marginally signiﬁcant preference

S.H. Sokolow et al. / Acta Tropica 132 (2014) 64–74 69

Prawn Size and consume large snails (>10 mm shell length). Population growth

Small Market rates remained near zero in the presence of prawns. In contrast, the

12.0 earliest recruits in the control tanks for all experiments appeared

within 10 days after stocking. The population growth rate in control

10.0

tanks was high, with peak abundances seen at 10–30 days for both

8.0

Biomphalaria and Bulinus populations (Fig. 6). After day 30, recruit-

6.0

ment began to wane and by 90 days, very few hatchlings were seen

by biomass (g) by

4.0 in either prawn or control tanks. By the end of the 90-day experi-

Selectivity index

2.0 ment, the prawn tanks had few new snails beyond those originally

stocked as founders, whereas the snail populations in control tanks

0.0

had increased by an order of magnitude and the adult egg-laying

2.0

population had quadrupled (for Biomphalaria) or tripled (for Buli-

nus). However, given that tanks with prawns had far fewer snails

1.5

overall, it was surprising to ﬁnd that the number of egg masses was

1.0 higher in the presence of prawns. By week 3, a difference could be

by number by

easily detected in the number of egg masses in prawn tanks and by

Selectivity index 0.5

the end of the 90-day experiment, prawn tanks contained an order

of magnitude more egg masses on average than control tanks for

0.0

both Biomphalaria (p = 0.02) and Bulinus (p = 0.008). In other words,

LMSLMS BG BT

small prawns led to an increase in egg laying or egg survival by

Snail size category Snail species adult snails, but nevertheless prevented eggs from recruiting into

the snail population.

Fig. 4. Results of preference trials for Small (<3 g) and Market sized (>30 g) M. rosen-

Manual removal of snail recruits (by crushing weekly, experi-

bergii prawns when offered either single species populations of B. glabrata snails of

ment 3c) resulted in similar outcomes compared with the effect

three size classes (S = 4 mm ± 2 mm, M = 8 mm ± 2 mm, L = 12 mm ± 2 mm) or two

snail species (BT = B. truncatus, BG = B. glabrata) in equal ratios. Outcomes are sim- of prawns, in terms of both snail population growth and stand-

ilar whether expressed in terms of biomass of snails consumed (top graph) or the ing egg numbers (Fig. 7). That is, recruitment of hatchling snails

number of snails consumed (bottom graph).

was blocked by either the addition of prawns or manual snail

recruit removal, but egg masses accumulated in both treatments

exhibited for B. truncatus over B. glabrata, (Fig. 4). To rule out any at a similar rate, which was much higher than in controls. This sug-

effect of snail size on inter-species preference measurements, we gests that the main mechanism by which prawn treatments led to

investigated selectivity indices for B. truncatus versus B. glabrata higher numbers of snail eggs was by reduction of the density of

on a subset of the data with only size-matched snails (medium B. snail recruits, so that small prawns, paradoxically, had a positive

truncatus versus medium B. glabrata). In this case, the selectivity effect on eggs (Fig. 8). Tanks with one rather than three prawns

indices for B. truncatus remained signiﬁcantly higher than for B. had intermediate numbers of eggs, suggesting a dose-response

glabrata (sign test: p = 0.04). When considering only size-matched relationship between the number of prawns (and hence the rate

snails, an odds ratio of attack probabilities for Biomphalaria com- of recruit removal by predation) and the standing stock of snail

pared with Bulinus was 0.37 (CI = 0.17–0.85) showing some factors eggs in the tanks. Despite the fact that snails in all the tanks were

other than size differences may be contributing to the preferences fed lettuce ad libitum, egg masses accumulated faster in the tanks

observed. The observed preference could theoretically alter the with shrimp feed supplementation, even without prawns, demon-

effectiveness of control for Bulinus versus Biomphalaria snails and strating an additional, direct effect of high quality (protein- and

therefore S. mansoni versus S. haematobium carried by each snail calorie-rich) food supplementation on snail fecundity.

species, respectively.

4. Discussion

3.4. Functional response

The results of our experiments indicate that M. vollenhovenii

For each prawn-species-size/snail-species-size category, the

and M. rosenbergii prawns are voracious predators of snails, hatch-

relationship between snail density and the number of snails con-

lings, and eggs, even in the presence of alternative food sources

sumed was ﬁt to Eq. (2) using non-linear least squares regression. A

(e.g., a commercial pelleted shrimp diet offered at a dry weight

Type II, or saturating functional response, ﬁt the data well (Fig. 5).

of 3–5% of prawn wet weight per day). Prawns consumption rates

Both attack rate a and handling time Th, were highly predictable

were predictable based on prawn size, snail size, and snail density.

given the ratio of prawn to snail body mass, with attack rate directly

These data ﬁll a critical gap in knowledge concerning the rate at

proportional to, and handling time inversely proportional to, the

which prawns can consume snails and their functional response

ratio of the two masses. Below a 3:1 ratio of prawn to snail body

to increasing or decreasing snail density, important parameters for

mass, prawns usually attacked zero snails, demonstrating a thresh-

predicting the regulatory effect of prawns on natural snail popu-

old of ∼30% of their own body weight above which snails were

lations. The results presented here will provide information which

perceived as too large to attack. These data suggest a predictable

can be useful, once validated with ﬁeld data, to investigate the efﬁ-

size refuge for the largest snails in the face of predation risk by small

cacy of using prawns as biological control agents to reduce parasite

prawns, which was observed commonly in our experiments and in

transmission to people.

previous studies (Roberts and Kuris, 1990).

3.5. Regulation of laboratory populations of Biomphalaria and 4.1. Satiation-limitation caused predictable functional responses

Bulinus snails among prawns of all sizes

In experiment 3b, small prawns prevented recruitment in snail During the functional response experiments performed here,

populations for at least 90 days by consuming small snails, hatch- all prawns consumed many more small than large snails when

lings, and/or eggs despite their inability (or unwillingness) to attack presented with single-sized populations at all densities. These

70 S.H. Sokolow et al. / Acta Tropica 132 (2014) 64–74

Fig. 5. (A) A subset of best ﬁt functional response curves, based on least squares ﬁtting of Holling’s disc equation for prawns of different size (Small = 1–3 g prawns,

Medium = 3–10 g prawns, Market = >30 g prawns) consuming B. glabrata snails of different size classes (8 mm or 12 mm ± 2 mm shell length). (B) The relationship between

the parameters governing the attack rate and handling time and prawn:snail body mass ratio, showing a predictable functional response. Data for M. vollenhovenii and M.

rosenbergii preying on either B. glabrata or B. truncatus were combined to generate this ﬁgure.

data suggest that digestion and satiation are limiting factors in 4.3. Prawns suppressed snail recruitment and fecundity, but the

ingestion rates. Satiation-limitation caused a predictable saturat- smallest prawns caused paradoxical trophic interactions in

ing functional response in the face of increasing snail densities, with laboratory snail populations

saturation determined by the total biomass consumed, rather than

the total number consumed. Satiation- or digestion-limitation is Large prawns rapidly consumed all sizes of snails presented

the most common type of limitation among predators, and many to them, strongly suppressing snail numbers, egg numbers, and

other crustaceans follow this pattern (Konan et al., 2010). Based on recruitment rates, with the potential to rapidly extinguish dense

our data, the parameters controlling the attack rate a and “handling snail populations within weeks. Large snails in the presence of

time” Th, two aggregate parameters that govern the overall shape small prawns, on the other hand, experienced a size refuge which

and asymptotic maximum of the functional response curve, were caused complex trophic interactions that regulated snail fecundity

highly predictable based on the ratio of prawn-mass:snail-mass and recruitment in unexpected ways (Fig. 8). Paradoxically, small

(Fig. 5). These data will facilitate parameterization of mechanistic prawns caused a striking increase in the standing stock of snail

models of schistosomiasis transmission that include biologically- eggs in tanks, even though a separate experiment showed they efﬁ-

realistic trophic interactions between predators and snail prey, not ciently consumed eggs, when tested in isolation, separated from

previously addressed in schistosomiasis models to date. Including other snails (see supplemental Fig. 1). Because this paradoxical

trophic interactions in schistosomiasis models will allow calcula- effect could, theoretically, reduce prawn efﬁcacy for snail control,

tion of the optimal predator (prawn) stocking and harvesting rate we speculate a bit further on why this occurs in our laboratory stud-

needed for effective biological control. ies. One explanation may be that competition for limiting resources

such as food, oxygen or micronutrients (Chernin and Michelson,

1957; Coelho et al., 1975; Loreau and Baluku, 1987; Mishkin and

Jokinen, 1986) between juvenile and adult snails led to lower fecun-

4.2. Preferences for Bulinus over Biomphalaria were detected dity in the adults when juveniles were not removed by predation

among prawns or crushing. Alternatively, it is possible that juvenile Biomphalaria

and Bulinus snails, like many aquatic snails, are egg cannibals; that

The slight preference for B. truncatus snails compared with B. is, in tanks with prawns, where many small snails were removed, a

glabrata demonstrated in the laboratory may be explained, in part, reduction of egg cannibalism by snails may have caused a trophic

by the differing shell morphology of the two snail species: Bulinus cascade, leading to a high standing stock of snail eggs (Fig. 8).

have thinner shells with relatively larger apertures, compared with The applicability of this laboratory ﬁnding to ﬁeld conditions

Biomphalaria, perhaps making it easier for prawns to access snail remains to be determined; it is unclear whether removal of snail

tissue by ﬂipping the snails over and reaching through the aperture. recruits by predation will lead to an increase in snail eggs in the

Other behavioral differences and other unmeasured determinants presence of small prawns in natural settings. It may be that egg can-

of preference may be at work as well, such as visual or chemical nibalism by juvenile snails or competition between juveniles and

cues or differences in shell crush resistance or defensive behavior adults are more likely in the laboratory setting, where low habitat

by the snails. complexity and high snail densities facilitate high egg-encounter

S.H. Sokolow et al. / Acta Tropica 132 (2014) 64–74 71

Fig. 6. Results of 90-day population regulation experiments using very small M. vollenhovenii (0.5–2 g) prawns. Shown are the trajectories over time for snail eggs (A,E),

hatchlings (B, F), juveniles (C, G), and new adults, not including the founding population (D,H) in prawn-treatment (solid lines) and control tanks (dashed lines). Small prawns

strongly suppressed recruitment, despite their inability to consume adult snails, even with an increased standing biomass of snail eggs. Snails began to hatch at day 10 and

then passed through successive size cohorts until they reached adult size by day 40–50.

rates and strong competition for resources. On the other hand, both of the prawns by the local native human populations might inter-

cannibalism and resource limitation have been shown to be com- fere with their effectiveness as control agents (Jordan, 1985). We

mon features among many terrestrial and aquatic animals in the argue exactly the opposite: it is precisely because prawns are a valu-

wild (Fox, 1975; Hairston et al., 1960; Polis, 1981; Wise, 2006) and able human food commodity that their re-introduction might offer

other natural snail populations have been shown to be regulated the most effective, feasible, and economically sustainable option

by egg-cannibalistic interactions, suggesting a possible importance for biological control in some rural locations. Our results support

of these complex trophic interactions in the ﬁeld (Baur, 1988). this hypothesis by demonstrating that young, growing prawns (too

Additional studies are needed to distinguish whether cannibalism small for harvest) have the most efﬁcient snail-killing ability. Max-

or competition or both are mechanisms underlying the observed imal snail consumption per gram prawn was seen in the mid-sized

patterns and whether these mechanisms are at work under ﬁeld prawns. The pattern that intermediate-sized prawns consumed

conditions. more than the largest or smallest prawns can be explained by two

factors: (1) at the smallest sizes, prawns are limited by lack of

4.4. Considering Macrobrachium prawns for biological control of strength or insufﬁcient mouth part size and are unable or unwill-

schistosomiasis ing to attack large snails, reducing their consumption rates overall;

however, (2) at the largest sizes, prawns approach their asymp-

Based on our laboratory ﬁndings, aquaculture-based restocking totic maximum size and thus growth slows and molting occurs less

of native Macrobrachium prawns warrants serious consideration as frequently, reducing consumption. Removal of the largest prawns

a biological control strategy for schistosomiasis, although future through harvest might actually increase snail control because

ﬁeld trials to validate our results are recommended before draw- the threat of large prawns cannibalizing smaller ones would be

ing conclusions about feasibility in the ﬁeld. Although the idea that reduced.

river prawns may control schistosomiasis has been suggested in If our results are validated in the ﬁeld, it is then plausible that

the past (Jordan, 1985; Lee et al., 1982; Roberts and Kuris, 1990), a regional scheme could be devised whereby revenue generated

the idea was mostly dismissed based on the argument that fishing by fishing or harvest of the largest prawns (>30 g) could finance

72 S.H. Sokolow et al. / Acta Tropica 132 (2014) 64–74 A 8 ab 7 a 6 bc 5 4 c 3 2 1 c

# egg masses/ adult snail 0

removal

3 prawns food only

neg control

single prawn Fig. 8. Proposed trophic interactions between large or small prawns and adult snails,

snail recruits, and snail eggs. Large prawns have negative direct and indirect effects

B on all snail life stages. On the other hand, small prawns (<2 g) are limited in their

ability to kill adult snails. A negative effect of juvenile recruit snails on eggs (due

20 b to competitive or egg-cannibalistic effects) led to positive indirect effects of small

prawns on snail eggs, despite a strong negative effect on snail recruitment.

15 ab

commodity, increasing the likelihood that their cultivation would

10 be ﬁnancially feasible and scalable. In Senegal, for example, the

price of large prawns is more than twice the price of ﬁsh in the

local markets. Lastly, M. vollenhovenii prawns have the advantage

5 that they are a native inhabitant of the river in large areas of Africa

a where schistosomiasis is endemic. It is interesting to note that

a the M. vollenhovenii used in our experiments were collected from

total # recruits/ adult snail # recruits/ total 0

the Lobe River, situated in the South Region of Cameroon, where

these native prawns are abundant (Brummett et al., 2008; Gabche

and Hockey, 1995) and schistosomiasis prevalence is relatively low

removal

3 prawns food only (Ratard et al., 1990). It is not clear if prawns or other factors, such

neg control

single prawn as low human population density or differences in rainfall, water

ﬂow, ecology, and the predominant schistosome and snail species

Fig. 7. Effect of ﬁve treatments on (A) snail fecundity (egg masses/adult snail)

in the South, are responsible for the relatively low schistosomia-

and (B) recruitment (new snail recruits/adult snail) in laboratory populations of

sis rates there (Greer et al., 1990). Nevertheless, it is possible that

Biomphalaria pfeifferi snails. “Removal” = manual snail recruit removal (by crushing

others of the more than 240 named species in the genus Macro-

weekly) plus 0.15 g shrimp diet added daily; “3 prawns” = 3 M. vollenhovenii prawns

(0.5–2 g each) housed/tank plus 0.15 g shrimp diet added daily, “single prawn” = 1 brachium distributed throughout the world (De Grave and Fransen,

M. vollenhovenii prawn (0.5–2 g) housed/tank plus 0.15 g of shrimp diet added daily, 2011) could be tested for their snail control beneﬁts and, if proven

food only = 0.15 g shrimp diet added daily (no prawns or recruit removal), and neg

effective, cultivated where their native ranges overlap with schisto-

control = a negative control whereby snails were only fed lettuce ad libitum. Bars

somiasis endemic regions, especially where their populations have

sharing a letter are not signiﬁcantly different.

been recently reduced by dams.

We recommend further consideration of prawns for biological

aquaculture and re-introduction of smaller prawns into the cohort control of schistosomiasis. Our studies show that prawns are effec-

at schistosomiasis transmission sites. Therefore, maintaining a captive at controlling snails under laboratory conditions and if this is

tive prawn broodstock for mass rearing of larval prawns, releasing also true in the ﬁeld setting, they may offer a novel, ecologically

them into net pens or “free range” (in the open waterways) along restorative and sustainable control strategy for schistosomiasis in

rivers and canals near transmission sites, could have simultaneous endemic regions. Large-scale ﬁeld trials to introduce prawns into

economic and disease control beneﬁts for local communities. net enclosures at transmission sites in Senegal are underway to

Biological control of snail populations using predators has test whether our laboratory results are scalable and applicable

received little attention by the public health community since the under ﬁeld conditions. A meta-analysis of schistosomiasis rates

drug praziquantel became widely available in the 1980’s. There in Africa showed that the risk of infection was elevated for peo-

have been limited successes using molluscivorous ﬁsh predators ple living near dams and irrigation schemes compared with those

for biological control of schistosome-susceptible snails in the past, far from these schemes throughout much of Sub-Saharan Africa

such as Serranochromis macrocephala in Central Africa (Adewale (Steinmann et al., 2006). Although speculative, we suppose many

and Afolayan, 2004), snail-eating cichlids in Lake Malawi (Slootweg other dam sites have similarly excluded some freshwater prawns

et al., 1994), and Oreochromis niloticus (larger adults only) in upriver, as apparently occurred in Senegal, and these dams may

Cameroon (Etim and Sankare, 1998). Prawns have beneﬁts over offer wider opportunities for testing whether prawn restoration or

other biological control agents such as ﬁsh because prawns can prawn aquaculture at transmission sites can decrease schistoso-

penetrate dense vegetation, or exit the water for brief periods miasis. Additionally, although ﬁne-scale data on prawn densities

(Baumgartner, 2003), allowing them access to snails where other are scarce, investigating the distribution of schistosomiasis rates in

ﬁsh predators are excluded. In addition, prawns fetch a higher regions where prawn populations are naturally abundant and not

price per kilogram than ﬁsh in most markets as a human food excluded by dams could be useful.

S.H. Sokolow et al. / Acta Tropica 132 (2014) 64–74 73

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Morphometric variation among male populations of freshwater shrimp Macro-

was supported by Award Number K08AI082284 from the National

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